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Abstract

Since Darwin’s time, waterbirds have been considered an important vector for the dispersal of continental aquatic invertebrates. Bird movements have facilitated the worldwide invasion of the American brine shrimp Artemia franciscana, transporting cysts (diapausing eggs), and favouring rapid range expansions from introduction sites. Here we address the impact of bird migratory flyways on the population genetic structure and phylogeography of A. franciscana in its native range in the Americas. We examined the sequence variation for two mitochondrial gene fragments (COI and 16S for a subset of the data) in a large set of population samples representing the entire native range of A. franciscana. Furthermore, we performed Mantel tests and redundancy analyses (RDA) to test the role of flyways, geography and human introductions on the phylogeography and population genetic structure at a continental scale. A. franciscanamitochondrial DNA was very diverse, with two main clades, largely corresponding to Pacific and Atlantic populations, mirroring American bird flyways. There was a high degree of regional endemism, with populations subdivided into at least 12 divergent, geographically restricted and largely allopatric mitochondrial lineages, and high levels of population structure ( Φ ST of 0.92), indicating low ongoing gene flow. We found evidence of human-mediated introductions in nine out of 39 populations analysed. Once these populations were removed, Mantel tests revealed a strong association between genetic variation and geographic distance (i.e., isolation-by-distance pattern). RDA showed that shared bird flyways explained around 20% of the variance in genetic distance between populations and this was highly significant, once geographic distance was controlled for. The variance explained increased to 30% when the factor human introduction was included in the model. Our findings suggest that bird-mediated transport of brine shrimp propagules does not result in substantial ongoing gene flow; instead, it had a significant historical role on the current species phylogeography, facilitating the colonisation of new aquatic environments as they become available along their main migratory flyways.

Author Comment

This is a preprint of an article submitted for formal peer review at PeerJ.

Additional Information

Competing Interests

There are no competing interests.

Author Contributions

Joaquín Muñoz conceived and designed the experiments, performed the experiments, analyzed the data, contributed reagents/materials/analysis tools, wrote the paper.

Africa Gómez conceived and designed the experiments, analyzed the data, wrote the paper.

DNA Deposition

The following information was supplied regarding the deposition of DNA sequences:

Sequences are currently being processed by GenBank (COI Accession Numbers: KF662951-KF663043, 16S still unavailable).

Data Deposition

The following information was supplied regarding the deposition of related data:

We plan to deposit alignments and input files for RDA analysis in Dryad.

Funding

AG was supported by a National Environment Research Council (NERC) Advanced Fellowship (NE/B501298/1). JM was supported by a Junta de Andalucía Excelence Project (P07-RNM-02511) and a European Science Foundation (ESF) grant awarded from the Research Networking Program Activity (ConGenOmics - EX/3646). AJG's sampling work in Canada was supported by a mobility grant from the Spanish Ministry of Science and Innovation (PR2008-0293) and help from M.T. Bidwell, and was otherwise supported by the Ministerio de Ciencia e Innovación (Project CGL2010-16028, including FEDER funds). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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